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Developmental trap or demographic bonanza? Opposing consequences of earlier phenology in a changing climate for a multivoltine butterfly
Abstract
A rapidly changing climate has the potential to interfere with the timing of environmental cues that ectothermic organisms rely on to initiate and regulate life history events. Short‐lived ectotherms that exhibit plasticity in their life history could increase the number of generations per year under warming climate. If many individuals successfully complete an additional generation, the population experiences an additional opportunity to grow, and a warming climate could lead to a demographic bonanza. However, these plastic responses could become maladaptive in temperate regions, where a warmer climate could trigger a developmental pathway that cannot be completed within the growing season, referred to as a developmental trap. Here, we incorporated detailed demography into commonly used photothermal models to evaluate these demographic consequences of phenological shifts due to a warming climate on the formerly widespread, multivoltine butterfly (Pieris oleracea). Using species‐specific temperature‐ and photoperiod‐sensitive vital rates, we estimated the number of generations per year and population growth rate over the set of climate conditions experienced during the past 38 years. We predicted that populations in the southern portion of its range have added a fourth generation in recent years, resulting in higher annual population growth rates (demographic bonanzas). We predicted that populations in the northeastern US have experienced developmental traps, where increases in the thermal window initially caused mortality of the final generation and reduced growth rates. These populations may recover if more growing degree days are added to the year. Our framework for incorporating detailed demography into commonly used photothermal models demonstrates the importance of using both demography and phenology to predict consequences of phenological shifts.
... Newly introduced insects can experience mismatches between the number of generations attempted based on photoperiod-induced diapause and the potential number of generations that could be possible with a well-adapted photoperiodic response (Bean et al. 2007, Grevstad andCoop 2015). Attempting reproduction too late in the year could lead to high mortality as life stages unable to diapause confront winter or senescing host plants (Van Dyck et al. 2015, Kerr et al. 2020. Entering diapause too early in the growing season can lead to greater overwintering mortality because of the added duration of diapause over the summer (Bean et al. 2007). ...
... Estimations of critical photoperiods may be used in combination with developmental degree-day requirements to predict voltinism at a given location over time (Beck and Apple 1961, Tobin et al. 2008, Kerr et al. 2020. The relationship of a population's mean critical photoperiod to modeled voltinism for a given climate and latitude has been covered in detail in Grevstad and Coop (2015). ...
... vary over short distances at similar latitudes (Lindestad et al. 2019). Insect phenology models that incorporate demography along with photoperiod-based diapause can estimate annual fitness for a particular critical photoperiod (Kerr et al. 2020), and extending these models across years could answer whether a critical photoperiod has reached an optimum for a population's environment (similar to trait models in Kivelä et al. 2013). ...
A key knowledge gap in classical biological control is to what extent insect agents evolve to novel environments. The introduction of biological control agents to new photoperiod regimes and climates may disrupt the coordination of diapause timing that evolved to the growing season length in the native range. We tested whether populations of Galerucella calmariensis L. have evolved in response to the potential mismatch of their diapause timing since their intentional introduction to the United States from Germany in the 1990s. Populations collected from 39.4° to 48.8° latitude in the western United States were reared in growth chambers to isolate the effects of photoperiod on diapause induction and development time. For all populations, shorter day lengths increased the proportion of beetles that entered diapause instead of reproducing. The critical photoperiods, or the day length at which half of a population diapauses, differed significantly among the sampled populations, generally decreasing at lower latitudes. The latitudinal trend reflects changes in growing season length, which determines the number of generations possible, and in local day lengths, at the time when beetles are sensitive to this cue. Development times were similar across populations, with one exception, and did not vary with photoperiod. These results show that there was sufficient genetic variation from the two German source populations to evolve different photoperiod responses across a range of environmental conditions. This study adds to the examples of rapid evolution of seasonal adaptations in introduced insects.
... Under a warming climate, populations which were formerly thermally restricted in parts of their range may be capable of producing an additional generation within the extended growing season (Kozak et al., 2019;Grevstad & Coop, 2015;Mitton & Ferrenberg, 2012;Altermatt 2010;Tobin et al., 2008) which could be beneficial or detrimental for populations. Species that can successfully add a generation in the extended growing season may benefit from another bout of reproduction, leading to higher overall population growth rates (Kerr et al., 2020;Kerr et al., 2019), and the potential for more rapid evolutionary responses to climate change (Chevin et al., 2010). In spite of its potential benefits, an increase in voltinism can also be detrimental to insects. ...
... For example, Satyrdotes appalachia (Appalachian Brown, Fig. 1b) may be transitioning from univoltine to bivoltine in our region (Stichter, 2015). If additional generations are the causal mechanism between changes in flight period and increased abundance in multivoltine species, it would suggest that beneficial effects of higher population growth rates (Kerr et al., 2020) and/or more rapid evolution (Chevin et al., 2010) outweigh the potential costs of developmental traps (Van Dyck et al., 2015;Levy et al., 2015). In general, multivoltine butterfly species seem to have higher population growth rates than univoltine species in north-temperate climates (MacGregor et al., 2019;Wepprich et al., 2019;Breed et al., 2013). ...
... Our results highlight the potential for phenological changes to affect population dynamics, and the general importance of phenological flexibility for insect population dynamics in changing environments. Past studies of phenology have rarely evaluated shifts in the end of activity (Zipf al., 2017;Gallinat et al., 2015), despite the demographic importance of late-season events such as entry into diapause (Kerr et al. 2020). Unlike traditional metrics of phenological change, quantile regression (Cade and Noon, 2003) enabled us to estimate trends in both the onset and end of flight across Massachusetts butterflies. ...
Phenological shifts are well‐documented in the ecological literature. However, their significance for changes in demography and abundance is less clear. We used 27 years of citizen science monitoring to quantify trends in phenology and relative abundance across 89 butterfly species. We calculated shifts in phenology using quantile regression and shifts in relative abundance using list length analysis and counts from field trips. Elongated activity periods within a year were the strongest predictor of increases in relative abundance. These changes may be driven in part by changes in voltinism, as this association was stronger in multivoltine species. Some species appear to be adding a late‐season generation, whereas other species appear to be adding a spring generation, revealing a possible shift from vagrant to resident. Our results emphasise the importance of evaluating phenological changes throughout species’ flight period and understanding the consequences for such climate‐related changes on viability or population dynamics.
... Under a warming climate, populations which were formerly thermally restricted in parts of their range may be capable of producing an additional generation within the extended growing season (Kozak et al., 2019;Grevstad & Coop, 2015;Mitton & Ferrenberg, 2012;Altermatt 2010;Tobin et al., 2008) which could be beneficial or detrimental for populations. Species that can successfully add a generation in the extended growing season may benefit from another bout of reproduction, leading to higher overall population growth rates (Kerr et al., 2020;Kerr et al., 2019), and the potential for more rapid evolutionary responses to climate change (Chevin et al., 2010). In spite of its potential benefits, an increase in voltinism can also be detrimental to insects. ...
... For example, Satyrdotes appalachia (Appalachian Brown, Fig. 1b) may be transitioning from univoltine to bivoltine in our region (Stichter, 2015). If additional generations are the causal mechanism between changes in flight period and increased abundance in multivoltine species, it would suggest that beneficial effects of higher population growth rates (Kerr et al., 2020) and/or more rapid evolution (Chevin et al., 2010) outweigh the potential costs of developmental traps (Van Dyck et al., 2015;Levy et al., 2015). In general, multivoltine butterfly species seem to have higher population growth rates than univoltine species in north-temperate climates (MacGregor et al., 2019;Wepprich et al., 2019;Breed et al., 2013). ...
... Our results highlight the potential for phenological changes to affect population dynamics, and the general importance of phenological flexibility for insect population dynamics in changing environments. Past studies of phenology have rarely evaluated shifts in the end of activity (Zipf al., 2017;Gallinat et al., 2015), despite the demographic importance of late-season events such as entry into diapause (Kerr et al. 2020). Unlike traditional metrics of phenological change, quantile regression (Cade and Noon, 2003) enabled us to estimate trends in both the onset and end of flight across Massachusetts butterflies. ...
... orchids in Norway [34] or yellow-bellied marmots in the US [35]), but markedly decreased growth rates of others (e.g. mustard white butterflies in the US [36]). Interestingly, these discrepancies might illuminate an interaction between phenology and demography that makes a wide array of responses more tractable, which is gaining attention [35][36][37][38][39][40][41]. ...
... mustard white butterflies in the US [36]). Interestingly, these discrepancies might illuminate an interaction between phenology and demography that makes a wide array of responses more tractable, which is gaining attention [35][36][37][38][39][40][41]. ...
... orchids in Norway [34] or yellow-bellied marmots in the US [35]), but markedly decreased growth rates of others (e.g. mustard white butterflies in the US [36]). Interestingly, these discrepancies might illuminate an interaction between phenology and demography that makes a wide array of responses more tractable, which is gaining attention [35][36][37][38][39][40][41]. ...
... mustard white butterflies in the US [36]). Interestingly, these discrepancies might illuminate an interaction between phenology and demography that makes a wide array of responses more tractable, which is gaining attention [35][36][37][38][39][40][41]. ...
Phenology refers to the seasonal timing patterns commonly exhibited by life on Earth, from blooming flowers to breeding birds to human agriculture. Climate change is altering abiotic seasonality (e.g. longer summers) and in turn, the phenological patterns contained within. However, how phenology evolves is still an unsolved problem. This problem lies at the crux of predicting future phenological changes that will likely have substantial ecosystem consequences, and more fundamentally, of understanding an undoubtedly global phenomenon. Most studies have associated proximate environmental variables with phenological responses in ways that are case-specific, making it difficult to contextualize observed changes within a general evolutionary framework. We advocate for general theory of phenological evolution centered around constructing null hypotheses to explain the disparate cases of phenological change in a systematic manner, and to distinguish when cases are surprising, and why. We outline the necessarily complex but universal ways in which timing within seasonal windows map onto evolutionary fitness. Throughout, we borrow lessons from life history theory and evolutionary demography that have benefited from a more first principles-based theoretical scaffold. Lastly, we identify key questions for theorists and empiricists to help synthesize and advance our general understanding of phenology.
... Second, many North American solitary bee species are in decline LeCroy et al., 2020), and we want to understand the causes of these declines. Changes in phenology can have positive impacts on insect populations (Duchenne, Thébault, Michez, Gérard, et al., 2020;Macgregor et al., 2019;Michielini et al., 2021), including matching of life cycles to new environmental conditions (Bonoan et al., 2021) and the possibility for additional generations in multivoltine species (Kerr et al., 2020). However, there are also notable examples of shifts having negative impacts on population viability, due to mismatches between altered phenology and interacting species (Kudo & Ida, 2013) or environmental cues for different life cycle events (Van Dyck et al., 2015). ...
... This finding is consistent with previous studies in Lepidoptera showing increases in flight duration through time(Altermatt, 2010a;Hodgson et al., 2011;Michielini et al., 2021). One hypothesis in Lepidoptera is that species are adding additional generations in response to longer growing seasons(Kerr et al., 2020). Climate also influences life cycle length in solitary bees. ...
Across taxa, the timing of life history events (phenology) is changing in response to warming temperatures. However, little is known about drivers of variation in phenological trends among species. We analyzed 168 years of museum specimen and sighting data to evaluate patterns of phenological change in 70 species of solitary bees that varied in three ecological traits: diet breadth (generalist or specialist), seasonality (spring, summer, or fall), and nesting location (above‐ or below‐ground). We estimated changes in onset, median, end, and duration of each bee species’ annual activity (flight duration) using quantile regression. To determine whether ecological traits could explain phenological trends, we compared average trends across species groups that differed in a single trait. We expected that specialist bees would be constrained by their host plants’ phenology and would show weaker phenological change than generalist species. We expected phenological advances in spring and delays in summer and fall. Lastly, we expected stronger shifts in above‐ground versus below‐ground nesters. Across all species, solitary bees have advanced their phenology by 0.43 days/decade. Since 1970, this advancement has increased four‐fold to 1.62 days/decade. Solitary bees have also lengthened their flight period by 0.44 days/decade. Seasonality and nesting location explained variation in trends among species. Spring‐ and summer‐active bees tended to advance their phenology, whereas fall‐active bees tended to delay. Above‐ground nesting species experienced stronger advances than below‐ground nesting bees in spring; however, the opposite was true in summer. Diet breadth was not associated with patterns of phenological change. Our study has two key implications. First, an increasing activity period of bees across the flight season means that bee communities will potentially provide pollination services for a longer period of time during the year. And, since phenological trends in solitary bees can be explained by some ecological traits, our study provides insight into mechanisms underpinning population viability of insect pollinators in a changing world.
... Climate change, in particular, is regarded as one of the main threats to biodiversity (Bellard et al. 2012), although for a number of species in cold environments it does in fact create new opportunities for population increases and range expansions (e.g., Menéndez et al. 2008;Pöyry et al. 2009). Rapid changes associated with climate change are expected in species such as insects with short life-cycles and high reproduction rates, whose populations can grow rapidly under favourable weather conditions (Kerr et al. 2019). However, in this type of species, unpredictable changes may also provoke sudden increases in mortality rates leading to population collapses and even extinctions (McLaughlin et al. 2002). ...
... Population growth was not explained by climatic region but was related to voltinism, with a higher frequency of negative effects recorded more frequently in univoltine species than in multivoltine ones both for temperature and rainfall variables. This finding is likely to be related to the poorer ability of single-generation species to recover in the same year from a negative climatic episode (Kerr et al. 2019). In addition, it suggests that univoltine species may suffer more severely under the current climate change scenario if it implies an increase in the frequency of the weather episodes we have identified as detrimental to population growth. ...
Understanding population responses to environmental conditions is key in the current context of climate change and the extreme climatic events that are threatening biodiversity in an unprecedented way. In this work, we provide a framework for understanding butterfly population responses to weather and extreme climatic seasons by taking into account topographic heterogeneity, species' life-cycles and density-dependent processes. We used a citizen-science database of Mediterranean butterflies that contains long-term population data (28 years) on 78 butterfly species from 146 sites in the Mediterranean mesic and alpine climate regions. Climatic data were obtained from 93 meteorological stations operating during this period near the butterfly sites. We studied how seasonal precipitation and temperature affect population growth while taking into account the effects of density dependence. Our results reveal (i) the beneficial effects of winter and spring precipitation for butterfly populations, which are most evident in the Mediterranean region and in univoltine species, and mainly affect the larval stage; (ii) a general negative effect of summer rain in the previous year, which affects the adult stage; and (iii) a consistent negative effect of mild autumns and winters on population growth. In addition, density dependence played a major role in the population dynamics of most species, except for those with long-term negative population trends. Our analyses also provide compelling evidence that both extreme population levels in previous years and extreme climatic seasons in the current year provoke population crashes and explosions, especially in the Mediterranean mesic region.
... First, it can reduce the time the immature stages need to develop, and thus, the time they are exposed to potential predators and parasitoids [20,21]. Second, it may increase the time available to complete generations, with potential benefits for abundance trends [22,23]. Finally, it may ensure good synchronization with the phenology of plants used as nectar sources, which are also expected to advance their flowering due to warming [24]. ...
... For instance, they could be detrimental if they lead to the addition of new generations that do not have enough time to enter diapause before the arrival of winter (i.e. developmental trap; [23,25]). Taken together, all these possible positive and negative effects involve great complexity to produce accurate predictions regarding the effects of changing the time of emergence on abundance trends. ...
Although climate-driven phenological shifts have been documented for many taxa across the globe, we still lack knowledge of the consequences they have on populations. Here, we used a comprehensive database comprising 553 populations of 51 species of northwestern Mediterranean butterflies to investigate the relationship between phenology and population trends in a 26-year period. Phenological trends and sensitivity to climate, along with various species traits, were used to predict abundance trends. Key ecological traits accounted for a general decline of more than half of the species, most of which, surprisingly, did not change their phenology under a climate warming scenario. However, this was related to the regional cooling in a short temporal window that includes late winter and early spring, during which most species concentrate their development. Finally, we demonstrate that phenological sensitivity-but not phenological trends-predicted population trends, and argue that species that best adjust their phenology to inter-annual climate variability are more likely to maintain a synchronization with trophic resources, thereby mitigating possible negative effects of climate change. Our results reflect the importance of assessing not only species' trends over time but also species' abilities to respond to a changing climate based on their sensitivity to temperature.
... In Sierra Nevada, the quality of nettles for supporting larval development decreased rapidly after having reached an optimum in May, and there was a long period of nearly 3 months starting in mid-June in which breeding opportunities were actually very low for this reason. Although the breeding season is curtailed and the higher growth rate that is typically linked to a multivoltine cycle is thus reduced (Kerr et al., 2020), we suggest that this loss is offset by higher larval survival resulting from lower parasitism. (Teder, 2020). ...
... Nevertheless, other explanations cannot be ruled out, as, for example, the poorer detectability of second generation adults if they enter into diapause soon after emergence. In any case, our results suggest that the predicted increase in the number of generations in multivoltine species under a scenario of climate warming(Altermatt, 2010;Kerr et al., 2020) could be constrained by the greater impact of parasitism in later generations. In fact, many species of butterflies and moths maintain a univoltine phenology throughout their European range even in the absence of thermal and phylogenetic constraints, suggesting that in some cases there are ecological constraints that make it disadvantageous to add additional generations even under a suitable climatic regime ...
1. Parasitism is a key factor in the population dynamics of many herbivorous insects, although its impact on host populations varies widely, for instance, along latitudinal and altitudinal gradients. Understanding the sources of geographical variation in host‐parasitoid interactions is crucial for reliably predicting the future success of the interacting species under a context of global change. 2. Here, we examine larval parasitism in the butterfly Aglais urticae in south‐west Europe, where it is a mountain specialist. Larval nests were sampled over two years along altitudinal gradients in three Iberian mountain ranges, including the Sierra Nevada, home to its southernmost European population. Additional data on nettle condition and adult butterflies were obtained in the study areas. 3. These data sources were used to investigate whether or not differences in parasitism rates are related to the geographical position and phenology of the host, and to the availability of the host plants. 4. Phenological differences in the host populations between regions were related to the severity of summer drought and the corresponding differences in host plant availability. At the trailing‐edge of its distribution, the butterfly’s breeding season was restricted to the end of winter and spring, while in its northern Iberian range the season was prolonged until mid‐summer. Although parasitism was an important source of mortality in all regions, parasitism rates and parasitoid richness were highest in the north and lowest in the south. Moreover, within a region, there was a notable increase in parasitism rates over time, which probably led to selection against an additional late‐summer host generation in northern regions. Conversely, the shorter breeding season in Sierra Nevada resulted in a loss of synchrony between the host and one important late‐season parasitoid, Sturmia bella, which may partly explain the high density of this butterfly species at the trailing‐edge of its range. 5. Our results support the key role of host phenology in accounting for differences in parasitism rates between populations. They also provide insights into how climate through host plant availability affects host phenology and, ultimately, the impact of parasitism on host populations.
... Seasonal plasticity is a classic example of a trait that can rapidly evolve in response to anthropogenic change and relies on the ability to use cues, such as photoperiod, to predict seasonal environmental changes. The relationship between cues and environmental changes can be easily disrupted by human activities, leading to developmental traps in which organisms produce inappropriate plastic phenotypes because of cue-environment mismatches (5,6). Research on climate change (7,8) and range-expanding invasive species (9)(10)(11) has shown that rapid evolution has the potential to correct for mismatches between photoperiodic cues and seasonality, at least in these contexts. ...
... Whereas the UHI is likely to directly select on phenology by altering seasonal weather conditions, ALAN may instead disrupt the ability to predict those conditions by altering daylength independently of the season itself. This could lead to a developmental trap in which organisms continue nondiapause development into winter conditions, with severe fitness consequences (5,6). For example, simulated ALAN substantially reduced diapause incidence in mosquito eggs and flesh fly pupae (20,21), although urban and Significance Cities represent novel environments with altered seasonality; they are warmer, which may accelerate growth, but light pollution can also lengthen days, misleading organisms that use daylength to predict seasonal change. ...
Significance
Cities represent novel environments with altered seasonality; they are warmer, which may accelerate growth, but light pollution can also lengthen days, misleading organisms that use daylength to predict seasonal change. Using long-term observational data, we show that urban populations of a butterfly and a moth have longer flight seasons than neighboring rural populations for six Nordic city regions. Next, using laboratory experiments, we show that the induction of diapause by daylength has evolved in urban populations in the direction predicted by urban warming. We thus show that the altered seasonality of urban environments can lead to corresponding evolutionary changes in the seasonal responses of urban populations, a pattern that may be repeated in other species.
... Elevated temperatures caused by climate change may stimulate the development of arthropods as well as increase the duration of the growing season, thereby increasing voltinism. In some cases, this may delay the induction of winter diapause, resulting in the production of an additional generation in autumn that cannot survive or enter diapause (i.e., the "lost generation hypothesis") [75][76][77]. Furthermore, if a chilling cue is not received, diapause expression may be delayed, reduced, or abandoned-causing individuals to emerge later or not at all [78]. ...
Climate change is expected to impact the global distribution and diversity of arthropods, with warmer temperatures forcing species to relocate, acclimate, adapt, or go extinct. The Arctic and Antarctic regions are extremely sensitive to climate change and have displayed profound and variable changes over recent decades, including decreases in sea ice extent, greening of tundra, and changes to hydrological and biogeochemical cycles. It is unclear how polar-adapted arthropods will respond to such changes, though many are expected to be at great risk of extinction. Here, we review the adaptive mechanisms that allow polar arthropods to persist in extreme environments and discuss how the effects of climate change at the poles will likely favour non-native species or those with the ability to rapidly evolve and/or acclimate. We find that physiological, behavioural, plastic, and genetic data are limited in scope for polar arthropods and research on adaptive responses to change is scarce. This restricts our ability to predict how they may respond to a warming climate. We call for a greater investment in research that specifically targets the ecology and evolution of these taxa, including genomic and transcriptomic approaches that can evaluate the potential for plastic and evolved environmental responses.
... In some cases, an extended period of warm temperatures that promotes development may delay winter diapause induction. This may create a developmental trap resulting in the production of a complete or partial additional generation in the autumn that cannot survive or enter diapause ("the lost generation hypothesis" (van Dyck et al., 2015;Kerr et al., 2020). In addition, diapause maintenance and termination are disrupted because of warm winters. ...
... Nevertheless, photoperiod is one aspect of the environment that does not change with 48 climate, and thus organisms that rely more heavily on photoperiod as a cue are predicted to 49 adjust their phenology less under climate change than species that rely on other, climate-50 sensitive cues (12). This can lead to inappropriate plastic responses to the new climate, with 51 potentially disastrous fitness consequences (13,14). Evolution of the photoperiodic reaction 52 norm for seasonal plasticity could correct for these mismatches and allow phenology to adjust 53 to the new climate. ...
Climate change alters seasonal environments without altering photoperiod, creating a cue-environment mismatch for organisms that rely on photoperiod as a cue for seasonal plasticity and phenology. Evolution can potentially correct for this mismatch by altering the photoperiodic reaction norm, but often phenology depends on multiple plastic decisions made at different life stages and times of year. We tested whether seasonal plasticity in different life stages evolves independently or in concert under climate change using Pararge aegeria (Speckled wood butterfly). This butterfly uses day length as a cue for life history plasticity in two different life stages: larval development time and pupal diapause. Photoperiodic reaction norms for plasticity in these traits were first measured over 30 years ago for two different Swedish populations. In this study, we replicated historic experiments that measured these reaction norms using the contemporary populations. We found evidence for evolution of the reaction norm for larval development time, but in opposite directions in the two populations. In contrast, we found no evidence for evolution of the reaction norm for pupal diapause. These results show that different life stages can evolve differently in response to climate change and only studying one part of the life cycle will not always be enough to fully understand how climate change impacts phenotypic plasticity and phenology.
... In some cases, an extended period of warm temperatures that promotes development may delay winter diapause induction. This may create a developmental trap resulting in the production of a complete or partial additional generation in the autumn that cannot survive or enter diapause ("the lost generation hypothesis" (van Dyck et al., 2015;Kerr et al., 2020). In addition, diapause maintenance and termination are disrupted because of warm winters. ...
Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects-central components of many ecosystems for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort.
... The timing of diapause is crucial in multivoltine populations (populations breeding more than one adult generation per growth season), where offspring born early in the growth season develop directly into adults, but later offspring enter diapause. Entering diapause too early in the summer is maladaptive because opportunities to reproduce are missed, and reproduction may fail completely if attempted too late in the autumn (Kerr et al., 2020;Van Dyck et al., 2015). Thus, it is unsurprising that local adaptation of responses to daylength is known in numerous insect species (Bean et al., 2012;Bradshaw & Holzapfel, 2007;Lindestad et al., 2019;Merckx et al., 2021;Tauber et al., 1986, pp. ...
Climate change allows species to expand polewards, but non‐changing environmental features may limit expansions. Daylength is unaffected by climate and drives life cycle timing in many animals and plants. Because daylength varies over latitudes, poleward‐expanding populations must adapt to new daylength conditions. We studied local adaptation to daylength in the butterfly Lasiommata megera, which is expanding northwards along several routes in Europe. Using common garden laboratory experiments with controlled daylengths, we compared diapause induction between populations from the southern‐Swedish core range and recently established marginal populations from two independent expansion fronts in Sweden. Caterpillars from the northern populations entered diapause in clearly longer daylengths than those from southern populations, with the exception of caterpillars from one geographically isolated population. The northern populations have repeatedly and rapidly adapted to their local daylengths, indicating that the common use of daylength as seasonal cue need not strongly limit climate‐induced insect range expansions. Many species that expand polewards as a result of climate change need to adapt to latitudinal differences in daylength because daylength guides life history decisions. We describe two parallel northward range expansions of a butterfly in Sweden and show experimentally that range margin populations at both expansion fronts have adapted locally to daylength. This has happened despite theory suggesting constraints to local adaptation at range margins and implies that the need to evolve new responses to daylength cues need not hinder range‐expansions.
... Accurate and precise phenological metrics of butterflies are of urgent concern given reports of broad butterfly declines [56][57][58] and recent results suggesting phenological shifts are associated with overall abundance trends 26,59 . Warmer temperatures are also leading to additional generations in certain multivoltine butterfly species, which may lead to unexpected shifts in median phenology, as well as affecting demographic outcomes 60 . While the focus here has been on early season and median timing across broad spatial and taxonomic scales, enhanced ability to capture number of broods over a season using incidental reporting or, better yet, integrated with structured survey data, may be possible but require new analytical approaches. ...
Data availability limits phenological research at broad temporal and spatial extents. Butterflies are among the few taxa with broad-scale occurrence data, from both incidental reports and formal surveys. Incidental reports have biases that are challenging to address, but structured surveys are often limited seasonally and may not span full flight phenologies. Thus, how these data source compare in phenological analyses is unclear. We modeled butterfly phenology in relation to traits and climate using parallel analyses of incidental and survey data, to explore their shared utility and potential for analytical integration. One workflow aggregated “Pollard” surveys, where sites are visited multiple times per year; the other aggregated incidental data from online portals: iNaturalist and eButterfly. For 40 species, we estimated early (10%) and mid (50%) flight period metrics, and compared the spatiotemporal patterns and drivers of phenology across species and between datasets. For both datasets, inter-annual variability was best explained by temperature, and seasonal emergence was earlier for resident species overwintering at more advanced stages. Other traits related to habitat, feeding, dispersal, and voltinism had mixed or no impacts. Our results suggest that data integration can improve phenological research, and leveraging traits may predict phenology in poorly studied species.
... Beyond biological control introductions, phenology models that incorporate photoperiodism and quantitatively predict phenological mismatch are relevant for a variety of modern applications including assessing the risk of invasive pests, planning assisted migration or reintroduction programs for species of conservation concern, and evaluating regional suitability for photoperiodcued crop plants. For established resident species, these models could be used to assess population vulnerability (or resilience) to global climate trends and climate variability and to predict near term booms or busts (please refer to Kerr et al. (2020) and Tobin et al. (2008) for some related examples). Finally, understanding how thermal and photoperiod responses interact to influence phenology is key to understanding the selective forces and potential for adaptation (i.e., evolutionary rescue) for populations facing changes in climate, whether that change results from transport to new regions, annual climate variability, or gradual global change. ...
A wide variety of organisms use the regular seasonal changes in photoperiod as a cue to align their life cycles with favorable conditions. Yet the phenological consequences of photoperiodism for organisms exposed to new climates are often overlooked. We present a conceptual approach and phenology model that maps voltinism (generations per year) and the degree of phenological mismatch that can arise when organisms with a short‐day diapause response are introduced to new regions or are otherwise exposed to new climates. Our degree‐day‐based model combines continent‐wide spatialized daily climate data, calculated date‐ and latitude‐specific day lengths, and experimentally determined developmental responses to both photoperiod and temperature. Using the case of the knotweed psyllid Aphalara itadori, a new biological control agent being introduced from Japan to North America and Europe to control an invasive weed, we show how incorporating a short‐day diapause response will result in geographic patterns of attempted voltinism that are strikingly different from the potential number of generations based on degree‐days alone. The difference between the attempted and potential generations represents a quantitative measure of phenological mismatch between diapause timing and the end of the growing season. We conclude that insects moved from lower to higher latitudes (or to cooler climates) will tend to diapause too late, potentially resulting in high mortality from inclement weather, and those moved from higher to lower latitude (to warmer climates) may be prone to diapausing too early, thus not fully exploiting the growing season and/or suffering from insufficient reserves for the longer duration in diapause. Mapped output reveals a central region with good phenology match that shifts north or south depending on the geographic source of the insect and its corresponding critical photoperiod for diapause. These results have direct relevance for efforts to establish populations of classical biocontrol agents. More generally, our approach and model could be applied to a wide variety of photoperiod‐ and temperature‐sensitive organisms that are exposed to changes in climate, including resident and invasive agricultural pests and species of conservation concern.
... Accurate and precise phenological metrics of butter ies are of urgent concern given reports of broad butter y declines [ [54][55][56] ] and recent results suggesting phenological shifts are associated with overall abundance trends [ 57,58 ]. Warmer temperatures are also leading to additional generations in certain multivoltine butter y species, which may lead to varying demographic outcomes [ 59 ]. While the focus here has been on emergence and median timing across broad spatial and taxonomic scales, enhanced ability to capture number of broods over a season using incidental reporting or, better yet, integrated with structured survey data, may be possible but require new analytical approaches. ...
Data availability limits phenological research at broad temporal and spatial extents. Butterflies are among the few taxa with broad-scale occurrence data, from both incidental reports and formal surveys. Incidental reports have observation biases that are challenging to address, but structured surveys are often limited seasonally and may not span full flight phenologies. Thus, which data source is more useful for phenological analyses is unclear. We use parallel analyses of incidental and survey data to determine how traits and climate drive phenological patterns for common butterflies. One workflow aggregated “Pollard” surveys, where sites are visited multiple times per year; the other aggregated incidental data from online portals: iNaturalist and eButterfly. For 40 routinely observed resident species, we estimated early (10%) and mid (50%) flight period metrics, and compared the spatiotemporal patterns and drivers of phenology across species and between datasets. Results were similar between datasets. Inter-annual variability was best explained by temperature, and seasonal emergence was earlier for resident species that overwinter at more advanced stages. Other traits had mixed or no impacts. The consistency in results suggests that data integration can improve phenological research, and leveraging traits may predict phenology in poorly studied species.
... Further, several recent papers have reported dramatic declines in insect populations (Hallmann et al., 2020;Wagner, 2020), potentially due to human-caused land-use change, climate change, introduced species and pollution (Wagner et al., 2021). Phenological shifts may exacerbate losses due to mismatches, but might provide a means to adapt to warmer temperatures and could even lead to overall population growth rates, particularly in species that can successfully add a generation due to extended growing seasons (Kerr et al., 2020). ...
Insect phenological lability is key for determining which species will adapt under environmental change. However, little is known about when adult insect activity terminates and overall activity duration. We used community-science and museum specimen data to investigate the effects of climate and urbanisation on timing of adult insect activity for 101 species varying in life history traits. We found detritivores and species with aquatic larval stages extend activity periods most rapidly in response to increasing regional temperature. Conversely, species with subterranean larval stages have relatively constant durations regardless of regional temperature. Species extended their period of adult activity similarly in warmer conditions regardless of voltinism classification. Longer adult durations may represent a general response to warming, but voltinism data in subtropical environments are likely underreported. This effort provides a framework to address the drivers of adult insect phenology at continental scales and a basis for predicting species response to environmental change.
... Further, several recent papers have reported dramatic declines in insect populations (Hallmann et al., 2020;Wagner, 2020), potentially due to human-caused land-use change, climate change, introduced species, and pollution (Wagner et al., 2021). Phenological shifts may exacerbate losses due to mismatches, but might provide a means to adapt to warmer temperatures and could even lead to overall population growth rates, particularly in species that can successfully add a generation due to extended growing seasons (Kerr et al., 2020). ...
Insect phenological lability is key for determining which species will adapt under environmental change. However, little is known about when adult insect activity terminates, and overall activity duration. We used community-science and museum specimen data to investigate the effects of climate and urbanization on timing of adult insect activity for 101 species varying in life history traits. We found detritivores and species with aquatic larval stages extend activity periods most rapidly in response to increasing regional temperature. Conversely, species with subterranean larval stages have relatively constant durations regardless of regional temperature. Multivoltine and univoltine species both extended their period of adult activity similarly in warmer conditions. Longer adult durations may represent a general response to warming, but voltinism data in subtropical environments is likely underreported. This effort provides a framework to address drivers of adult insect phenology at continental scales, and a basis for predicting species response to environmental change.
... For example, deviations from optimal thermal developmental conditions have negative consequences, as they can cause a mismatch in the timing of maturation (i.e. 'developmental trap', Boggs, 2016;Kerr et al., 2020;Van Dyck, Bonte, Puls, Gotthard, & Maes, 2015), affect final body size with cascading effects for adult life histories, and even impact survival (Douhard et al., 2013;e.g. ;Jannot, 2009;Orizaola, Dahl, & Laurila, 2010;Pankhurst & Munday, 2011). ...
Cold developmental conditions can greatly affect adult life history of ectotherms in seasonal habitats. Such effects are mostly negative, but sometimes adaptive. Here, we tested how cold conditions experienced during pupal development affect adult wing melanization of an insect ectotherm, the Glanville fritillary butterfly, Melitaea cinxia. We also assessed how in turn previous cold exposure and increased melanization can shape adult behaviour and fitness, by monitoring individuals in a seminatural set-up. We found that, despite pupal cold exposure inducing more melanization, wing melanization was not linked to adult thermoregulation preceding flight, under the conditions tested. Conversely, wing-vibrating behaviour had a major role in producing heat preceding flight. Moreover, more melanized individuals were more mobile across the experimental set-up. This may be caused by a direct impact of melanization on flight ability or a more indirect impact of coloration on behaviours such as mate search strategies and/or eagerness to disperse to more suitable mating habitats. We also found that more melanized individuals of both sexes had reduced mating success and produced fewer offspring, which suggests a clear fitness cost of melanization. Whether the reduced mating success is dictated by impaired mate search behaviour, reduced physical condition leading to a lower dominance status or weakened visual signalling remains unknown. In conclusion, while there was no clear role of melanization in providing a thermal advantage under our seminatural conditions, we found a fitness cost of being more melanized, which potentially impacted adult space use behaviour.
... Diapause is usually induced by short daylengths that are typical for the end of the growth season and are consequently used as a cue of the future harsh conditions of winter [5, 96,104]. The adaptive value of photoperiodic induction relies on historical correlations between photoperiod and climatic variables such as temperature and precipitation, and rapid climate change will distort these correlations leading to inappropriate diapause timing [105,106]. (Figure 3). ...
Overwintering is a serious challenge for insects, and winters are rapidly changing as climate shifts. The capacity for phenotypic plasticity and evolutionary adaptation will determine which species profit or suffer from these changes. Here we discuss current knowledge on the potential and evidence for evolution in winter-relevant traits among insect species and populations. We conclude that the best evidence for evolutionary shifts in response to changing winters remain those related to changes in phenology, but all evidence points to cold hardiness as also having the potential to evolve in response to climate change. Predicting future population sizes and ranges relies on understanding to what extent evolution in winter-related traits is possible, and remains a serious challenge.
Effects of climate on forest insect populations are complex, often involving drivers that are opposing, nonlinear, and nonadditive. Overall, climate change is driving an increase in outbreaks and range shifts. Links between climate and forest insect dynamics are becoming clearer; however, the underlying mechanisms remain less clear. Climate alters forest insect population dynamics directly through life history, physiology, and voltinism, and indirectly through effects on host trees and natural enemies. Climatic effects on bark beetles, wood-boring insects, and sap suckers are often indirect, through effects on host tree susceptibility, whereas climatic effects on defoliators are comparatively more direct. We recommend process-based approaches to global distribution mapping and population models to identify underlying mechanisms and enable effective management of forest insects.
Phenology refers to the seasonal timing patterns commonly exhibited by life on Earth, from blooming flowers to breeding birds to human agriculture. Climate change is altering abiotic seasonality (e.g., longer summers) and in turn, phenological patterns contained within. However, how phenology should evolve is still an unsolved problem. This problem lies at the crux of predicting future phenological changes that will likely have substantial ecosystem consequences, and more fundamentally, of understanding an undeniably global phenomenon. Most studies have associated proximate environmental variables with phenological responses in case-specific ways, making it difficult to contextualize observations within a general evolutionary framework. We outline the complex but universal ways in which seasonal timing maps onto evolutionary fitness. We borrow lessons from life history theory and evolutionary demography that have benefited from a first principles-based theoretical scaffold. Lastly, we identify key questions for theorists and empiricists to help advance our general understanding of phenology.
Natural history collections (NHCs) have been indispensable to understanding longer‐term trends of the timing of seasonal events. Massive‐scale digitization of specimens promises to further enable phenological research, especially the ability to move towards a deeper understanding of drivers of change and how trait‐environment interactions shape phenological sensitivity. Despite the promise of NHCs to answer fundamental phenology questions, use of these data resources present unique and often overlooked challenges requiring specialized workflow steps, such as assembling multisource data, accounting for date imprecision, and making decisions about trade‐offs between data density and spatial resolution. We provide a set of key best practice recommendations and showcase these via a case study that utilizes NHC data to test hypotheses about spatiotemporal trends in adult Lepidoptera (i.e., butterflies and moths) flight timing across North America. Our case study is a worked example of these best practices, helping practitioners recognize and overcome potential pitfalls at each step, from data acquisition and cleaning, to delineating spatial units and proper estimation of phenological metrics and associated uncertainty, to building appropriate models. We confirm and extend the critical importance of voltinism and diapause strategy, but less‐so daily activity patterns, for predicting Lepidoptera phenology spatiotemporal trends. Our case study also showcases the unique power of NHC data to test existing hypotheses and generate new insights about temporal phenological trends. Specifically, migratory species and species that enter diapause as adults are advancing the start of flight periods in more recent years, even after accounting for climate context. These results highlight the physiological and adaptive differences between species with different overwintering strategies. We close by noting the value of partnerships between data scientists, museum experts, and ecological modelers to fully harness the power of digital data resources to address pressing global change challenges. These partnerships can extend approaches for integrating multiple data types to fully unlock our understanding of the tempo, mode, drivers, and outcomes of phenological changes at greater spatial, temporal, and taxonomic scales.
Predicting how species respond to changes in climate is critical to conserving biodiversity. Modeling efforts to date have largely centered on predicting the effects of warming temperatures on temperate species phenology. In and near the tropics, the effects of a warming planet on species phenology are more likely to be driven by changes in the seasonal precipitation cycle rather than temperature. To demonstrate the importance of considering precipitation-driven phenology in ecological studies, we present a case study wherein we construct a mechanistic population model for a rare subtropical butterfly (Miami blue butterfly, Cyclargus thomasi bethunebakeri) and use a suite of global climate models to project butterfly populations into the future. Across all iterations of the model, the trajectory of Miami blue populations is uncertain. We identify both biological uncertainty (unknown diapause survival rate) and climate uncertainty (ambiguity in the sign of precipitation change across climate models), and their interaction as key factors that determine persistence vs. extinction. Despite uncertainty, the most optimistic iteration of the model predicts that Miami blue butterfly populations will decline under the higher emissions scenario (RCP 8.5). The lack of climate model agreement across the projection ensemble suggests that investigations into the effect of climate change on precipitation-driven phenology require a higher level of rigor in the uncertainty analysis compared to analogous studies of temperature. For tropical species, a mechanistic approach that incorporates both biological and climate uncertainty is the best path forward to understand the effect shifting precipitation regimes have on phenology and population dynamics.
Global change includes multiple overlapping and interacting drivers: 1) climate change, 2) land use change, 3) novel chemicals, and 4) the increased global transport of organisms. Recent studies have documented the complex and counterintuitive effects of these drivers on the behavior, life histories, distributions, and abundances of insects. This complexity arises from the indeterminacy of indirect, non-additive and combined effects. While there is wide consensus that global change is reorganizing communities, the available data are limited. As the pace of anthropogenic changes outstrips our ability to document its impacts, ongoing change may lead to increasingly unpredictable outcomes. This complexity and uncertainty argue for renewed efforts to address the fundamental drivers of global change.
Life history trade‐offs are ubiquitous in nature. Life history theory posits that these trade‐offs arise from individuals having limited resources to allocate toward all vital functions, such as survival, growth and reproduction. These trade‐offs position most species along a slow‐fast life history continuum, where individuals with slow life histories often have higher survival at the cost of delayed reproduction and individuals with fast life histories often live faster and die younger. However, these trade‐offs are sometimes less obvious for invasive species. Here, we constructed age‐based population models to compare life history strategies and trade‐offs between the noninvasive, native mustard white and invasive, exotic cabbage white (Pieris spp.) butterflies. We found that the cabbage white has faster larval growth and higher fecundity at younger ages, suggesting it has a fast life history compared to the mustard white. However, cabbage white also has higher adult survival at younger ages, suggesting that it experiences weaker trade‐offs among vital rates than its native counterpart. Our study illustrates the importance of demographic studies in evaluating life history strategies among congener species with different population histories, and emphasizes the many advantages experienced by invasive species in their novel environments. Invasive species have many advantages over native species in their novel environments. Here, we found that the invasive cabbage white butterfly has weakened life history trade‐offs compared to its native counterpart, which challenges fundamental life history theory that organisms should exhibit trade‐offs among vital functions.
Advances in phenology (the annual timing of species’ life-cycles) in response to climate change are generally viewed as bioindicators of climate change, but have not been considered as predictors of range expansions. Here, we show that phenology advances combine with the number of reproductive cycles per year (voltinism) to shape abundance and distribution trends in 130 species of British Lepidoptera, in response to ~0.5 °C spring-temperature warming between 1995 and 2014. Early adult emergence in warm years resulted in increased within- and between-year population growth for species with multiple reproductive cycles per year (n = 39 multivoltine species). By contrast, early emergence had neutral or negative consequences for species with a single annual reproductive cycle (n = 91 univoltine species), depending on habitat specialisation. We conclude that phenology advances facilitate polewards range expansions in species exhibiting plasticity for both phenology and voltinism, but may inhibit expansion by less flexible species.
Significance
The biological consequences of climate change are determined by the responses of individual species and interactions among species. Hybridization, or interbreeding between related species, is an interaction that affects how species evolve in response to environmental change. Here we provide evidence that climatic warming has caused a geographic shift of a butterfly hybrid zone and that strong selection and/or genetic incompatibilities maintain species boundaries during this movement. Through simulations, we show that as climate change progresses, the rate and geographic configuration of future hybrid zone movement will vary across space and time. This geographic variation in future hybrid zone movement may lead to divergent ecological and evolutionary outcomes, and thus has implications for local conservation and management.
1.There are wide reports of advances in the timing of spring migration of birds over time and in relation to rising temperatures, though phenological responses vary substantially within and among species. An understanding of the ecological, life-history and geographic variables that predict this intra- and inter-specific variation can guide our projections of how populations and species are likely to respond to future climate change. 2.Here, we conduct phylogenetic meta-analyses addressing slope estimates of the timing of avian spring migration regressed on (i) year and (ii) temperature, representing a total of 413 species across five continents. We take into account slope estimation error and examine phylogenetic, ecological and geographic predictors of intra- and inter-specific variation. 3.We confirm earlier findings that on average birds have significantly advanced their spring migration time by 2.1 days decade(-1) and 1.2 days °C(-1) . We find that over time and in response to warmer spring conditions short-distance migrants have advanced spring migratory phenology by more than long-distance migrants. We also find that larger bodied species show greater advance over time compared to smaller bodied species. Our results did not reveal any evidence that interspecific variation in migration response is predictable on the basis of species' habitat or diet. 4.We detected a substantial phylogenetic signal in migration time in response to both year and temperature, suggesting that some of the shifts in migratory phenological response to climate are predictable on the basis of phylogeny. However, we estimate high levels of species and spatial variance relative to phylogenetic variance, which is consistent with plasticity in response to climate evolving fairly rapidly and being more influenced by adaptation to current local climate than by common descent. 5.On average, avian spring migration times have advanced over time and as spring has become warmer. While we are able to identify predictors that explain some of the true among-species variation in response, substantial intra- and inter-specific variation in migratory response remains to be explained. This article is protected by copyright. All rights reserved.
We developed an agent-based stochastic model expressing stage-specific phenology and population dynamics for an insect species across geographic regions. We used the invasive pentatomid, Halyomorpha halys, as the model organism because gaps in knowledge exist regarding its developmental physiology, it is expanding its global distribution, and it is of significant economic importance. Model predictions were compared against field observations over three years, and the parameter set that enables the largest population growth was applied to eight locations over ten years, capturing the variation in temperature and photoperiod profiles of significant horticultural crop production that could be affected by H. halys in the US. As a species that overwinters as adults, critical photoperiod significantly impacted H. halys seasonality and population size through its influence on diapause termination and induction, and this may impact other insects with similar life-histories. Photoperiod and temperature interactions influenced life stage synchrony among years, resulting in an order of magnitude difference, for occurrence of key life stages. At all locations, there was a high degree of overlap among life stages and generation. Although all populations produced F2 adults and thus could be characterized as bivoltine, the size and relative contribution of each generation to the total, or overwintering, adult population also varied dramatically. In about half of the years in two locations (Geneva, NY and Salem, OR), F1 adults comprised half or more of the adult population at the end of the year. Yearly degree-day accumulation was a significant covariate influencing variation in population growth, and average maximum adult population size varied by 10-fold among locations. Average final population growth was positive (Asheville, NC, Homestead, FL, Davis, CA) or marginal (Geneva, NY, Bridgeton, NJ, Salem, OR, Riverside, CA), but was negative in one location (Wenatchee WA) due to cooler temperatures coupled with timing of vitellogenesis of F2 adults. Years of the highest population growth in the mid-Atlantic site coincided with years of highest crop damage reports. We discuss these results with respect to assumptions and critical knowledge gaps, the ability to realistically model phenology of species with strongly overlapping life stage and which diapause as adults.
Insect responses to recent climate change are well documented, but the role of resource specialization in determining species vulnerability remains poorly understood. Uncovering local ecological effects of temperature change with high-quality, standardized data provides an important first opportunity for predictions about responses of resource specialists, and long-term time series are essential in revealing these responses. Here, we investigate temperature-related changes in local insect communities, using a sampling site with more than a quarter-million records from two decades (1992-2009) of full-season, quantitative light trapping of 1543 species of moths and beetles. We investigated annual as well as long-term changes in fauna composition, abundance and phenology in a climate-related context using species temperature affinities and local temperature data. Finally, we explored these local changes in the context of dietary specialization. Across both moths and beetles, temperature affinity of specialists increased through net gain of hot-dwelling species and net loss of cold-dwelling species. The climate-related composition of generalists remained constant over time. We observed an increase in species richness of both groups. Furthermore, we observed divergent phenological responses between cold- and hot-dwelling species, advancing and delaying their relative abundance, respectively. Phenological advances were particularly pronounced in cold-adapted specialists. Our results suggest an important role of resource specialization in explaining the compositional and phenological responses of insect communities to local temperature increases. We propose that resource specialists in particular are affected by local temperature increase, leading to the distinct temperature-mediated turnover seen for this group. We suggest that the observed increase in species number could have been facilitated by dissimilar utilization of an expanded growing season by cold- and hot-adapted species, as indicated by their oppositely directed phenological responses. An especially pronounced advancement of cold-adapted specialists suggests that such phenological advances might help minimize further temperature-induced loss of resource specialists. Although limited to a single study site, our results suggest several local changes in the insect fauna in concordance with expected change of larger-scale temperature increases.
Phenology shifts are the most widely cited examples of the biological impact of climate change, yet there are few assessments of potential effects on the fitness of individual organisms or the persistence of populations. Despite extensive evidence of climate-driven advances in phenological events over recent decades, comparable patterns across species' geographic ranges have seldom been described. Even fewer studies have quantified concurrent spatial gradients and temporal trends between phenology and climate. Here we analyse a large data set (~129 000 phenology measures) over 37 years across the UK to provide the first phylogenetic comparative analysis of the relative roles of plasticity and local adaptation in generating spatial and temporal patterns in butterfly mean flight dates. Although populations of all species exhibit a plastic response to temperature, with adult emergence dates earlier in warmer years by an average of 6.4 days per °C, among-population differences are significantly lower on average, at 4.3 days per °C. Emergence dates of most species are more synchronised over their geographic range than is predicted by their relationship between mean flight date and temperature over time, suggesting local adaptation. Biological traits of species only weakly explained the variation in differences between space-temperature and time-temperature phenologi-cal responses, suggesting that multiple mechanisms may operate to maintain local adaptation. As niche models assume constant relationships between occurrence and environmental conditions across a species' entire range, an important implication of the temperature-mediated local adaptation detected here is that populations of insects are much more sensitive to future climate changes than current projections suggest.
The impact of mutualists on a partner's demography depends on how they affect the partner's multiple vital rates and how those vital rates, in turn, affect population growth. However, mutualism studies rarely measure effects on multiple vital rates or integrate them to assess the ultimate impact on population growth. We used vital rate data, population models and simulations of long-term population dynamics to quantify the demographic impact of a guild of ant species on the plant Ferocactus wislizeni. The ants feed at the plant's extrafloral nectaries and attack herbivores attempting to consume reproductive organs. Ant-guarded plants produced significantly more fruit, but ants had no significant effect on individual growth or survival. After integrating ant effects across these vital rates, we found that projected population growth was not significantly different between unguarded and ant-guarded plants because population growth was only weakly influenced by differences in fruit production (though strongly influenced by differences in individual growth and survival). However, simulations showed that ants could positively affect long-term plant population dynamics through services provided during rare but important events (herbivore outbreaks that reduce survival or years of high seedling recruitment associated with abundant precipitation). Thus, in this seemingly clear example of mutualism, the interaction may actually yield no clear benefit to plant population growth, or if it does, may only do so through the actions of the ants during rare events. These insights demonstrate the value of taking a demographic approach to studying the consequences of mutualism.
Global climate change is causing shifts in phenology across multiple species. We use a geographically and temporally extensive data set of butterfly abundance across the state of Ohio to ask whether phenological change can be predicted from climatological data. Our focus is on growing degree days (GDD), a commonly used measure of thermal accumulation, as the mechanistic link between climate change and species phenology. We used simple calculations of median absolute error associated with GDD and an alternative predictor of phenology, ordinal date, for both first emergence and peak abundance of 13 butterfly species. We show that GDD acts as a better predictor than date for first emergence in nearly all species, and for peak abundance in more than half of all species, especially univoltine species. Species with less ecological flexibility, in particular those with greater dietary specialization, had greater predictability with GDD. The new method we develop for predicting phenology using GDD offers a simple yet effective way to predict species' responses to climate change.
The timing of many biological events, including butterfly imago emergence, has advanced under climate change, with the rate of these phenological changes often differing among taxonomic groups. Such inter-taxa variability can lead to phenological mismatches. For example, the timing of a butterfly’s flight period may become misaligned with a key nectar resource, potentially increasing the extinction risk to both species. Here we fit statistical models to field data to determine how the phenology of the marbled white butterfly, Melanargia galathea, and its main nectar source, greater knapweed, Centaurea scabiosa, have changed over recent years at three sites across the UK. We also consider whether topographical diversity affects C. scabiosa’s flowering period. At our focal site, on the species’ northern range limit, we find that over a 13-year period the onset of C. scabiosa’s flowering period has become later whilst there is no obvious trend over time in the onset of M. galathea’s flight period. In recent years, butterflies have started to emerge before their key nectar source was available across most of the site. This raises the intriguing possibility that phenological mismatch could be an unrecognised determinant of range limits for some species. However, the presence of topographical diversity within the site decreased the chance of a mismatch occurring by increasing the length of the flowering period by up to 14 days. We suggest that topographical diversity could be an important component in minimising phenological mismatches under future climate change.
Microclimate has been known to drive variation in the distribution and abundance of insects for some time. Until recently however, quantification of microclimatic effects has been limited by computing constraints and the availability of fine-scale biological data. Here, we tested fine-scale patterns of persistence/extinction in butterflies and moths against two computed indices of microclimate derived from Digital Elevation Models: a summer solar index, representing fine-scale variation in temperature, and a topographic wetness index, representing fine-scale variation in moisture availability. We found evidence of microclimate effects on persistence in each of four 20 × 20 km British landscapes selected for study (the Brecks, the Broads, Dartmoor, and Exmoor). Broadly, local extinctions occurred more frequently in areas with higher minimum or maximum solar radiation input, while responses to wetness varied with landscape context. This negative response to solar radiation is consistent with a response to climatic warming, wherein grid squares with particularly high minimum or maximum insolation values provided an increasingly adverse microclimate as the climate warmed. The variable response to wetness in different landscapes may have reflected spatially variable trends in precipitation. We suggest that locations in the landscape featuring cooler minimum and/or maximum temperatures could act as refugia from climatic warming, and may therefore have a valuable role in adapting conservation to climatic change.
Climate warming affects the rate and timing of the development in ectothermic organisms. Short-living, ectothermic organisms (including many insects) showing thermal plasticity in life-cycle regulation could, for example, increase the number of generations per year under warmer conditions. However, changed phenology may challenge the way organisms in temperate climates deal with the available thermal time window at the end of summer. Although adaptive plasticity is widely assumed in multivoltine organisms, rapid environmental change could distort the quality of information given by environmental cues that organisms use to make developmental decisions. Developmental traps are scenarios in which rapid environmental change triggers organisms to pursue maladaptive developmental pathways. This occurs because organisms
must rely upon current environmental cues to predict future environmental conditions and corresponds to a novel case of ecological or evolutionary traps. Examples of introduced, invasive species are congruent with this hypothesis. Based on preliminary experiments, we argue that the dramatic declines of the wall brown Lasiommata megera in northwestern Europe may be an example of a developmental trap. This formerly widespread, bivoltine (or even multivoltine) butterfly has become a conundrum to conservationist biologists. A split-brood field experiment with L. megera indeed suggests issues with life-cycle regulation decisions at the end of summer. In areas where the species went extinct recently, 100% of the individuals developed directly into a third generation without larval diapause, whereas only 42.5% did so in the areas where the species still occurs. Under unfavourable autumn conditions, the attempted third generation will result in high mortality and eventually a lost or ‘suicidal’ third generation in this insect with non-overlapping, discrete generations. We discuss the idea of a developmental trap within an integrated framework for assessing the vulnerability of species to climate change.
Many temperate insects take advantage of longer growing seasons at lower latitudes by increasing their generation number or voltinism. In some insects, development time abruptly decreases when additional generations are fit into the season. Consequently, latitudinal "sawtooth" clines associated with shifts in voltinism are seen for phenotypes correlated with development time, like body size. However, latitudinal variation in voltinism has not been linked to genetic variation at specific loci. Here we show a pattern in allele frequency among voltinism ecotypes of the European corn borer moth (Ostrinia nubilalis) that is reminiscent of a sawtooth cline. We characterized 145 autosomal and sex-linked SNPs and found that period, a circadian gene that is genetically linked to a major QTL determining variation in post-diapause development time, shows cyclical variation between voltinism ecotypes. Allele frequencies at an unlinked circadian clock gene cryptochrome1 were correlated with period. These results suggest that selection on development time to 'fit' complete life cycles into a latitudinally varying growing season produce oscillations in alleles associated with voltinism, primarily through changes at loci underlying the duration of transitions between diapause and other life history phases. Correlations among clock loci suggest possible coupling between the circadian clock and the circannual rhythms for synchronizing seasonal life history. We anticipate that latitudinal oscillations in allele frequency will represent signatures of adaptation to seasonal environments in other insects and may be critical to understanding the ecological and evolutionary consequences of variable environments, including response to global climate change. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Maximum likelihood or restricted maximum likelihood (REML) estimates of the
parameters in linear mixed-effects models can be determined using the lmer
function in the lme4 package for R. As for most model-fitting functions in R,
the model is described in an lmer call by a formula, in this case including
both fixed- and random-effects terms. The formula and data together determine a
numerical representation of the model from which the profiled deviance or the
profiled REML criterion can be evaluated as a function of some of the model
parameters. The appropriate criterion is optimized, using one of the
constrained optimization functions in R, to provide the parameter estimates. We
describe the structure of the model, the steps in evaluating the profiled
deviance or REML criterion, and the structure of classes or types that
represents such a model. Sufficient detail is included to allow specialization
of these structures by users who wish to write functions to fit specialized
linear mixed models, such as models incorporating pedigrees or smoothing
splines, that are not easily expressible in the formula language used by lmer.
Climate warming is expected to change the distribution and abundance of
many species. Range shifts have been detected in a number of European
taxa for which long-term government-initiated or organized-survey data
are available. In North America, well-organized long-term data needed to
document such shifts are much less common. Opportunistic observations
made by citizen scientist groups may be an excellent alternative to
systematic surveys. From 1992 to 2010, 19,779 butterfly surveys were
made by amateur naturalists in Massachusetts, a geographically small
state located at the convergence of northern and southern bioclimatic
zones in eastern North America. From these data, we estimated population
trends for nearly all butterfly species (100 of 116 species present)
using list-length analysis. Population trajectories indicate increases
of many species near their northern range limits and declines in nearly
all species (17 of 21) near their southern range limits. Certain
life-history traits, especially overwintering stage, were strongly
associated with declines. Our results suggest that a major,
climate-induced shift of North American butterflies, characterized by
northward expansions of warm-adapted and retreat of cold-adapted
species, is underway.
Reproductive diapause is common in the Chrysomelidae, and allows 'escape in time' of conditions unfavourable for growth and development. Chrysophtharta agricola (Chapuis) (Coleoptera : Chrysomelidae), which undergoes one or two generations per year, spends 7–8 months in reproductive diapause, emerging in spring to feed and oviposit. We manipulated photoperiod and temperature to test their effects on induction and termination of diapause in the laboratory; we also conducted field studies for validation of results, and to examine patterns of voltinism as determined by the onset of diapause. A critical photoperiod of between 12 and 16 h of light was required to initiate diapause in the laboratory and field, although 55% of beetles entered diapause in response to low temperature (9°C) alone. At short photoperiods (8L : 16D), high temperature (21°C) subverted diapause in 20% of adults. Therefore, voltinism in C. agricola is a seasonally plastic trait dependent on emergence time of teneral adults. Diapause termination was primarily influenced by temperature, although photoperiod had an effect at low temperatures. Beetles accumulated day-degrees (DD) during overwintering, with beetles collected later terminating diapause sooner than those collected earlier (total DD was similar). Diapause termination is, therefore, dependent on DD accumulation above the threshold temperature (6.7°C), rather than a specific environmental cue. Results are discussed in ecological and applied contexts, and provide the ability to predict the population phenology of C. agricola. Seasonal plasticity, as demonstrated here, allows insects to balance resource availability, reproductive strategy and climatic tolerance.
Caterpillars have a great capacity for rapid weight gain, but to reap the benefits of this capacity, larvae must be able to
survive in a hostile environment and emerge as adults at the right time of year. In this article, I review examples of growth
decisions in butterfly larvae that can be viewed as adaptations for optimized growth performance. These include sex-specific
growth decisions that lead to protandry and sexual size dimorphism, fine-tuning of growth in response to photoperiod and temperature,
development of alternative larval morphs that mimic the plant structures they feed on, and the peculiar growth patterns of
lycenid butterflies that manipulate ants and grow as “cuckoos” inside ant nests. I conclude that growth of an individual can
be seen as the sum of several environmentally dependent decisions, which may influence the growth trajectory by changes in
physiology, behavior, and morphology.
Synchronizing the annual timing of physiological, morphological, and behavioral transitions with seasons enables survival in temperate environments [1]. The capacity to adjust life history timing and track local seasonal cycles can facilitate geographic expansion [2], adaptation [3], and tolerance [4-6] during rapid environmental change. Understanding the proximate causes of variation in seasonal timing improves prediction of future response and persistence [7, 8]. However, relatively little is known about the molecular basis generating this diversity [9], particularly in Lepidoptera, a group with many species in decline [10, 11]. In insects, the stress-tolerant physiological state of diapause enables coping with seasonal challenges [1, 12-15]. Seasonal changes in photoperiod and temperature are used to synchronize diapause with winter, and timing of diapause transitions varies widely within and among species [9, 16]. Changes in spring diapause termination in the European corn borer moth (Ostrinia nubilalis) have allowed populations to respond to shorter winters and emerge ∼3 weeks earlier in the year [17]. Multiple whole-genome approaches suggest two circadian clock genes, period (per) and pigment-dispersing factor receptor (Pdfr), underlie this polymorphism. Per and Pdfr are within interacting quantitative trait loci (QTL) and differ in allele frequency among individuals that end diapause early or late, with alleles maintained in high linkage disequilibrium. Our results provide testable hypotheses about the physiological role of circadian clock genes in the circannual timer. We predict these gene candidates will be targets of selection for future adaptation under continued global climate change [18].
Every living creature on Earth is made of atoms of the various bioelements that are harnessed in the construction of molecules, tissues, organisms, and communities, as we know them. Organisms need these bioelements in specific quantities and proportions to survive and grow. Distinct species have different functions and life strategies, and have therefore developed distinct structures and adopted a certain combination of metabolic and physiological processes. Each species is thus also expected to have different requirements for each bioelement. We therefore propose that a “biogeochemical niche” can be associated with the classical ecological niche of each species. We show from field data examples that a biogeochemical niche is characterized by a particular elementome defined as the content of all (or at least most) bioelements. The differences in elementome among species are a function of taxonomy and phylogenetic distance, sympatry (the bioelemental compositions should differ more among coexisting than among non‐coexisting species to avoid competitive pressure), and homeostasis with a continuum between high homeostasis/low plasticity and low homeostasis/high plasticity. This proposed biogeochemical niche hypothesis has the advantage relative to other associated theoretical niche hypotheses that it can be easily characterized by actual quantification of a measurable trait: the elementome of a given organism or a community, being potentially applicable across taxa and habitats. The changes in bioelemental availability can determine genotypic selection and therefore have a feedback on ecosystem function and organization, and, at the end, become another driving factor of the evolution of life and the environment.
The seasonal cycle varies geographically, and organisms are under selection to express life cycles that optimally exploit their spatiotemporal habitats. In insects, this often means producing an annual number of generations (voltinism) appropriate to the local season length. Variation in voltinism may arise from variation in environmental factors (e.g. temperature or photoperiod) acting on a single reaction norm shared across populations, but it may also result from local adaptation of reaction norms. However, such local adaptation is poorly explored at short geographic distances, especially within latitudes. Using a combination of common‐garden rearing and life cycle modeling, we have investigated the causal factors behind voltinism variation in Swedish populations of the butterfly Pararge aegeria, focusing on a set of populations that lie within a single degree of latitude but nonetheless differ in season length and voltinism. Despite considerable differences in ambient temperature between populations, modeling suggested that the key determinant of local voltinism was in fact interpopulation differences in photoperiodic response. These include differences in the induction thresholds for winter diapause, as well as differences in photoperiodic regulation of larval development, a widespread but poorly studied phenomenon. Our results demonstrate previously neglected ways that photoperiodism may mediate insect phenological responses to temperature, and emphasize the importance of local adaptation in shaping phenological patterns in general, as well as for predicting the responses of populations to changes in climate. This article is protected by copyright. All rights reserved.
Understanding the correspondence between ambient temperature and insect development is necessary to forecast insect phenology under novel environments. In the face of climate change, both conservation and pest control efforts require accurate phenological predictions. Here, we compare a suite of degree‐day models to assess their ability to predict the phenology of a common, oligophagous butterfly, the silver‐spotted skipper, Epargyreus clarus (Cramer) (Lepidoptera: Hesperiidae). To estimate model parameters, we used development time of eggs and larvae reared in the laboratory at six constant temperatures ranging from 8 to 38 °C and on two host plants of contrasting quality (kudzu and wisteria). We employed three approaches to determine the base temperature to calculate degree days: linear regression, modified reduced major axis regression, and application of a generic base temperature value of 10 °C, which is commonly used in the absence of laboratory data. To calculate the number of degree days required to complete a developmental stage, we used data from caterpillars feeding on high‐ and low‐quality hosts, both in the field and in the laboratory. To test model accuracy, we predicted development time of seven generations of larvae reared in the field on the same host plants across 3 years (2014–2016). To compare performance among models, we regressed predicted vs. observed development time, and found that r2 values were significantly larger when accounting for host plant quality. The accuracy of development time predictions varied across the season, with estimates of the first two generations being more accurate than estimates of the third generation, when ambient temperatures dropped outside the range in which development rate and temperature have a linear relationship. Overall, we show that accounting for variation in host plant quality when calculating development time in the field is more important than the choice of the base temperature for calculating degree days. We evaluated a suite of degree‐day models for insect phenology developed and parameterized through various methodologies. To assess model performance we predicted the phenology of a multivoltine, oligophagous butterfly, silver‐spotted skipper, Epargyreus clarus (Lepidoptera: Hesperiidae), in the field over multiple years. We demonstrated that accounting for variation in host plant quality when calculating development time in the field was more important than the parameterization of the base temperature for calculating degree days.
Warming, crops, and insect pests
Crop responses to climate warming suggest that yields will decrease as growing-season temperatures increase. Deutsch et al. show that this effect may be exacerbated by insect pests (see the Perspective by Riegler). Insects already consume 5 to 20% of major grain crops. The authors' models show that for the three most important grain crops—wheat, rice, and maize—yield lost to insects will increase by 10 to 25% per degree Celsius of warming, hitting hardest in the temperate zone. These findings provide an estimate of further potential climate impacts on global food supply and a benchmark for future regional and field-specific studies of crop-pest-climate interactions.
Science , this issue p. 916 ; see also p. 846
Phenology is a first order control on productivity and mediates the biophysical environment by altering albedo, surface roughness length and evapotranspiration. Accurate and transparent modelling of vegetation phenology is therefore key in understanding feedbacks between the biosphere and the climate system. 2.Here, we present the phenor R package and modelling framework. The framework leverages measurements of vegetation phenology from four common phenology observation datasets, the PhenoCam network, the USA National Phenology Network (USA-NPN), the Pan European Phenology Project (PEP725), MODIS phenology (MCD12Q2) combined with (global) retrospective and projected climate data. 3.We show an example analysis using the phenor modelling framework which quickly and easily compares 20 included spring phenology models for three plant functional types. An analysis of model skill using the root mean squared (RMSE) error shows little or no difference regardless of model structure, corroborating previous studies. We argue that addressing this issue will require novel model development combined with easy data assimilation as facilitated by our framework. 4.In conclusion, we hope the phenor phenology modelling framework in the R language and environment for statistical computing will facilitate reproducibility and community driven phenology model development, in order to increase their overall predictive power, and leverage an ever growing number of phenology data products. This article is protected by copyright. All rights reserved.
The habitat of the green-veined white butterfly Pieris oleracea in eastern North America has undergone invasions by the exotic plant garlic mustard (Alliaria petiolata), which is replacing native hosts of P. oleracea such as Cardamine diphylla. A. petiolata was originally lethal to most larvae of the native butterfly but during the past 20+ years it has been incorporated successfully into the larval diet, likely through evolutionary change. The region was also invaded by another exotic plant, Cardamine pratensis, on which the native butterfly larvae readily develops, allowing the possibility of population rescue. Further complicating the butterfly's reproductive dynamics, it is multigenerational within a summer, and host plant availability and location change during the summer. Our goal is to model the expected dynamics of the native butterfly population in this evolving, dynamic landscape by using a new bio-inspired paradigm known as membrane computing.
Synopsis:
Historical data show that recent climate change has caused advances in seasonal timing (phenology) in many animals and plants, particularly in temperate and higher latitude regions. The population and fitness consequences of these phenological shifts for insects and other ectotherms have been heterogeneous: warming can increase development rates and the number of generations per year (increasing fitness), but can also lead to seasonal mismatches between animals and their resources and increase exposure to environmental variability (decreasing fitness). Insect populations exhibit local adaptation in their developmental responses to temperature, including lower developmental thresholds and the thermal requirements to complete development, but climate change can potentially disrupt seasonal timing of juvenile and adult stages and alter population fitness. We investigate these issues using a global dataset describing how insect developmental responds to temperature via two traits: lower temperature thresholds for development (T0) and the cumulative degree-days required to complete development (G). As suggested by previous analyses, T0 decreases and G increases with increasing (absolute) latitude; however, these traits and the relationship between G and latitude varies significantly among taxonomic orders. The mean number of generations per year (a metric of fitness) increases with both decreasing T0 and G, but the effects of these traits on fitness vary strongly with latitude, with stronger selection on both traits at higher (absolute) latitudes. We then use the traits to predict developmental timing and temperatures for multiple generations within seasons and across years (1970-2010). Seasonality drives developmental temperatures to peak mid-season and for generation lengths to decline across seasons, particularly in temperate regions. We predict that climate warming has advanced phenology and increased the number of generations, particularly at high latitudes. The magnitude of increases in developmental temperature varies little across latitude. Increases in the number of seasonal generations have been greatest for populations experiencing the greatest phenological advancements and warming. Shifts in developmental rate and timing due to climate change will have complex implications for selection and fitness in seasonal environments.
In monandrous mating systems with discrete nonoverlapping generations males should maximize the expected number of matings by starting to emerge before females. This is known as protandry. Moreover, Evolutionarily Stable Strategies (ESS) models show that the male emergence curve should be abruptly truncated before female emergence has ceased. In temperate areas where many insects have partial second generations, we accordingly predict that males should enter diapause development at an earlier date than should females, as a result of late-emerging males being penalized in terms of fewer mating opportunities. The decision to diapause or to develop directly is usually mediated by response to environmental stimuli of which day length is the most important. Hence we predict that the mechanism by which males enter diapause at an earlier date than females will be that of the male reaction norm for diapause development being shifted towards longer day lengths when compared to that of females. As a result of the greater tendency of males to enter diapause development, partial second generations that develop directly should be female biased. As a corollary, first generations should be male biased because some males of the first generation are from the previous year. The prediction that males should enter diapause development earlier in the season, i.e., at longer day lengths, as compared to females was corroborated by rearing Pieris napi under a variety of critical day length regimes producing mixed broods of directly developing and diapausing individuals, and by outdoor rearings of cohorts of larvae of P. napi and P. rapae initiated throughout the season. The prediction that partial second generations should be female biased was corroborated by laboratory rearings at constant temperature of P. napi (Pieridae), Polygonia c-album (Nymphalidae), and Pararge aegeria (Satyridae) under critical day length conditions, producing female-biased sex ratio under direct, and male-biased sex ratio under diapause development.
Synthesizing papers from the last two years, I examined generalizations about the fingerprints of climate change on insects’ population dynamics and phenology. Recent work shows that populations can differ in response to changes in climate means and variances. The part of the thermal niche occupied by an insect population, voltinism, plasticity and adaptation to weather perturbations, and interactions with other species can all exacerbate or mitigate responses to climate change. Likewise, land use change or agricultural practices can affect responses to climate change. Nonetheless, our knowledge of effects of climate change is still biased by organism and geographic region, and to some extent by scale of climate parameter.
Insect phenologies are changing in response to climate warming. Shifts toward earlier seasonal activity are widespread; however, responses of insect phenology to warming are often more complex. Many species have prolonged their activity periods; others have shown delays. Furthermore, because of interspecific differences in temperature sensitivity, warming can increase or decrease synchronization between insects and their food plants and natural enemies. Here, I review recent findings in three areas — shifts in phenology, changes in voltinism, and altered species interactions — and highlight counterintuitive responses to warming caused by the particularities of insect life cycles. Throughout, I emphasize how an appreciation of the evolutionary processes shaping insect life histories is necessary to forecast changes in insect phenology and their demographic consequences.
Photoperiodism comprises a miscellany of clock phenomena in which the organisms distinguish the long days or short nights of summer from the short days or long nights of autumn and winter and, thereby obtain information on calendar time from the environment. This chapter describes the principal photoperiodic phenomena observed in insects. In classical photoperiodism, the insects are able to distinguish between the long days or short nights of summer and the short days or long nights of autumn and respond with a seasonally appropriate switch in metabolism. Photoperiodic switches control diapause, seasonal morphs, growth rates, and a variety of associated physiological states. Diapause involves a temporary inactivation or alteration of the endocrine system, triggered by the appropriate photoperiodic stimulus acting on the brain. In a few insects, however, the diapause state is imposed by a diapause hormone or by a particular hormone titre. Quiescence differs from diapause in the sense that it is the direct response to adverse environmental conditions, for example, dehydration or cold torpor.
Management of at-risk species requires attention to species-specific resource requirements. In butterflies, lack of information on resource selection in adults limits conservation. We investigated nectar plant use and selection by Fender's blue butterfly (Plebejus [= Icaricia] icarioides fenderi), a species endangered by loss of over 99% of prairie habitat in Oregon's Willamette Valley, USA. We observed 156 male and 75 female nectaring bouts by Fender's blue at 3 sites across the range of the species concurrent with weekly surveys of nectar availability. Overall, 53% of nectar uses by males and 20% of uses by females were on non-native species. Of the 24 plant species used by males and females, 8 species accounted for 86% of uses. Tests of resource selection (Wilkes λ) using compositional analysis for these 8 species were significant, indicating that nectar resources were used selectively, rather than in proportion to availability. Females selected native nectar species over non-native species, whereas patterns for males were less clear. This study highlights the importance of differentiating between males and females when examining habitat requirements for endangered species. In addition, understanding how specific non-native species are used by endangered species will help managers decide when they should be removed or conserved. © 2015 The Wildlife Society.
1.Understanding the drivers of population abundance across species and sites is crucial for effective conservation management. At present, we lack a framework for predicting which sites are likely to support abundant butterfly communities.2.We address this problem by exploring the determinants of abundance among 1111 populations of butterflies in the UK, spanning 27 species on 54 sites. Our general hypothesis is that the availability of food resources is a strong predictor of population abundance both within and between species, but that the relationship varies systematically with species’ traits.3.We found strong positive correlations between butterfly abundance and the availability of food resources. Our indices of hostplant and nectar are both significant predictors of butterfly population density, but the relationship is strongest for hostplants, which explain up to 36% of the intersite variance in abundance for some species.4.Among species, the hostplant–abundance relationship is mediated by butterfly species traits. It is strongest among those species with narrow diet breadths, low mobility and habitat specialists. Abundance for species with generalist diet and habitat associations is uncorrelated with our hostplant index.5.The hostplant–abundance relationship is more pronounced on sites with predominantly north-facing slopes, suggesting a role for microclimate in mediating resource availability.6.Synthesis and applications. We have shown that simple measures can be used to help understand patterns in abundance at large spatial scales. For some butterfly species, population carrying capacity on occupied sites is predictable from information about the vegetation composition. These results suggest that targeted management to increase hostplant availability will translate into higher carrying capacity. Among UK butterflies, the species that would benefit most from such intervention have recently experienced steep declines in both abundance and distribution. The hostplant–abundance relationship we have identified is likely to be transferrable to other systems characterized by strong interspecific interactions across trophic levels. This raises the possibility that the quality of habitat patches for specialist species is estimable from rapid assessment of the hostplant resource.This article is protected by copyright. All rights reserved.
A change in climate is known to affect seasonal timing (phenology) of the life stages of poikilothermic organisms whose development depends on temperature. Less understood is the potential for even greater disruption to the life cycle when a phenology shift exposes photoperiod-sensitive life stages to new day lengths. We present a conceptual framework and model to investigate the ways that photoperiod-cued diapause can interact with a change in climate or latitude to influence voltinism in poikilothermic organisms. Our degree-day phenology model combines detailed spatial climate data, latitude-and date-specific photoperiods, and development and photoperiod response parameters. As an example, we model the biological control beetle Galerucella calmariensis and map the number of generations expected following its introduction into diverse climates throughout the continental United States. Incorporation of photoperiodism results in a complex geography of voltinism that differs markedly from predictions of traditional phenology models. Facultative multivoltine species will be prone to univoltism when transported to either warmer or southern climates due to exposure of the sensitive stage to shorter day lengths. When moved to more northern locations, they may attempt too many generations for the season duration thereby exposing vulnerable life stages to harsh weather in the fall. We further show that even small changes in temperature can result in large and unexpected shifts in voltinism. Analogous effects may be expected for organisms from wide variety of taxa that use photoperiod as a seasonal cue during some stage of their life cycle. Our approach is useful for understanding the performance and impacts of introduced pests and beneficial organisms as well as for predicting responses of resident species to climate change and climate variability.
The native pierid butterfly Pieris oleracea underwent a large range reduction in New England in the twentieth century, likely due to the introduction the invasive butterfly Pieris rapae (Lep.: Pieridae) to North America in 1860, and later the oligophagous parasitoid Cotesia glomerata (Hymenoptera: Braconidae) in 1884. Thought extirpated from the state by the 1970s, one large dense population of the butterfly was found in the mid 1980s in a flood plain meadow along the Housatonic River in Lenox, Berkshire Co., Massachusetts. We examined how this native pierid was able to maintain a relatively dense local population by feeding on a novel, invasive host plant, Cardamine pratensis (cuckoo flower), in a meadow habitat despite known parasitoid presence. We approached this question in three ways. First, we deployed trap host plants (cuckoo flower and collards) stocked host larvae (first and second instars of either P. rapae or P. oleracea) at the Lenox site and other locations to determine current rates of C. glomerata attack, for comparison with historical information. Second, we used olfactometer experiments to determine if C. glomerata females could detect the cuckoo flower volatiles released during P. oleracea larval feeding. Third, we used field-cage experiments to determine if the plant architecture found in the flood plain meadow inhibited the ability of C. glomerata females to locate and parasitize hosts. Specifically, we asked if overtopping vegetation prevented or reduced parasitism of P. oleracea larvae feeding on the covered basal rosettes of C. pratensis, which is the physical form of host plant for three of the four butterfly generations at the site.
The oviposition behavior of two montane Pieris butterfly species is described and discussed in relation to potential evolution of foodplant utilization. Oviposition behavior toward several crucifer species was examined in relation to 1) larval growth requirements; 2) the relative abundances of these species; 3) preferences of individual females; and 4) the spatial distribution of these species. Free-flying female butter-flies were followed in three outdoor observation areas and their consecutive oviposition choices were recorded. The relative abundance of crucifers and their spatial distribution were determined in these areas. Females oviposit on nearly all available Cruciferae. Oviposition preferences tend to reflect the suitability of crucifers for larval growth, but females do not always accurately assess the suitability of a crucifer species for larval growth. Although it is not possible to exclude oviposition specialists which preferentially exploit one or two of several potential larval food resources, there is little evidence for their existence in these butterfly populations. Individual females appear, over time, to utilize all crucifer species exploited by the population as a whole, but consecutive choices may be influenced by the patchy spatial distribution of crucifer species. It is suggested that the imprecise correspondence between adult oviposition behavior and larval growth requirements may be due to 1) historical factors, and 2) habitat heterogeneity, and may provide impetus for improved food-seeking abilities in larvae.
Aim We investigate the importance of interacting species for current and potential future species distributions, the influence of their ecological characteristics on projected range shifts when considering or ignoring interacting species, and the consistency of observed relationships across different global change scenarios.
Location Europe.
Methods We developed ecological niche models (generalized linear models) for 36 European butterfly species and their larval host plants based on climate and land-use data. We projected future distributional changes using three integrated global change scenarios for 2080. Observed and projected mismatches in potential butterfly niche space and the niche space of their hosts were first used to assess changing range limitations due to interacting species and then to investigate the importance of different ecological characteristics.
Results Most butterfly species were primarily limited by climate. Species dwelling in warm areas of Europe and tolerant to large variations in moisture conditions were projected to suffer less from global change. However, a gradient from climate to host plant control was apparent, reflecting the range size of the hosts. Future projections indicated increased mismatching of already host-plant-limited butterflies and their hosts. Butterflies that utilize plants with restricted ranges were projected to suffer most from global change. The directions of these relationships were consistent across the scenarios but the level of spatial mismatching of butterflies and their host plants increased with the severity of the scenario.
Main conclusions Future changes in the co-occurrence of interacting species will depend on political and socio-economic development, suggesting that the composition of novel communities due to global change will depend on the way we create our future. A better knowledge of ecological species characteristics can be utilized to project the future fate and potential risk of extinction of interacting species leading to a better understanding of the consequences of changing biotic interactions. This will further enhance our abilities to assess and mitigate potential negative effects on ecosystem functions and services.
In north-eastern Italy, the second-generation larvae of Lobesia botrana (Den. & Schiff.) (Lepidoptera: Tortricidae) can develop with two different time patterns. In particular, in ‘warmer’ areas, the developmental time is shorter than in ‘cooler’ areas and it is associated with an earlier and more economically important third generation.Because the differences in temperature are not sufficient to explain the two patterns, research was carried out aiming to investigate whether the differences in larval development time are the result of a different number of instars and whether the photoperiod is a factor.In the field, second-generation larvae develop through five instars in a ‘warmer’ area and through six instars in a ‘cooler’ area. Laboratory and field data showed that decreasing photoperiod, which induces diapause, is also an important cue for inducing larvae to develop six instars.In the light of climate warming and subsequent changes in L. botrana phenology over the last 30 years, the two different development patterns are interpreted as a means to ensure the best fit of the moth to environmental conditions. In ‘cooler’ areas, third-generation larvae might not complete development before frost or harvest, and hence second-generation larvae develop through six instars before producing overwintering pupae.
Climate warming accelerates the timing of flowering and insect pollinator emergence, especially in spring. If these phenological shifts progress independently between species, features of plant-pollinator mutualisms may be modified. However, evidence of phenological mismatch in pollination systems is limited. We investigated the phenologies of a spring ephemeral, Corydalis ambigua, and its pollinators (bumble bees), and seed-set success over 10-14 years in three populations. Although both flowering onset and first detection of overwintered queen bees in the C. ambigua populations were closely related to snowmelt time and/or spring temperature, flowering tended to be ahead of first pollinator detection when spring came early, resulting in lower seed production owing to low pollination service. Relationships between flowering onset time, phenological mismatch, and seed-set success strongly suggest that phenological mismatch is a major limiting factor for reproduction of spring ephemerals. This report demonstrates the mechanism of phenological mismatch and its ecological impact on plant-pollinator interactions based on long-term monitoring. Frequent occurrence of mismatch can decrease seed production and may affect the population dynamics of spring ephemerals.
Phenology models play an important role in insect ecology and pest management. For bark beetle species prone to frequent outbreaks, they help predict swarming periods, discern sister generations hard to recognize in the field yet indispensable in studies of bark beetle population dynamics, predict the extent to which the generations entering diapause develop, as well as help address the omnipresent issue of impacts of climate change. As a prerequisite to developing a simulation model of landscape-level forest disturbances in the Bohemian Forest, including those due to Ips typographus, we validate the phenology model PHENIPS, published in the literature and simulating seasonal development of this species, by data coming from this region. We find a reasonable agreement between the modeled and actually observed bark beetle dynamics, thus strengthening the potential role of PHENIPS in any future attempt to model dynamics of Central European populations of I. typographus. In addition, we use PHENIPS to assess impacts of climate change on temperature-regulated phenology of I. typographus. In contrast to previous studies which used regional climate models to predict future temperature development, we independently account for changes in the mean air temperature and in the frequency of extreme weather events – for the latter, we assume that the inter-annual air temperature variance will also increase. Since bark beetle development is driven by bark temperatures and both low and high bark temperatures inhibit the development, we find that the effects of increases in the air temperature mean and variance are compensatory. Hence, if climate is to change so that both these characteristics grow, we expect only a relatively minor change in generation development time. Moreover, initiation of the third filial generation of I. typographus in the Bohemian Forest is predicted to occur only for relatively large shifts in the mean air temperature.
Interactions of two sympatric, closely related Pieris species, indigenous P. oleracea and naturalized P. rapae, are described. The spatial and temporal distribution of adults and juveniles indicates broad overlap, but each species occupies a habitat or utilizes a foodplant not successfully exploited by the other. Pieris oleracea utilizes indigenous Dentaria diphylla, a woodland crucifer, and flies in wooded areas rarely occupied by P. rapae; P. rapae utilizes naturalized Barbarea vulgaris, which is usually lethal to P. oleracea larvae. Although potential for interspecific competition is substantial, there is no evidence for ecological displacement. Crop rotation and undisturbed woodland promote growth of crucifers that support large open populations of both species. No evidence of reproductive interference was observed. These observations suggest that composition and abundance of the crucifer flora are more important than interspecific interactions in determining Pieris abundance and ecological distributi...
Pieris napi oleracea Harris is a native pierid butterfly whose range in New England has decreased since the 1869 invasion of an exotic congener, Pieris rapae (L.). Populations have disappeared from all but a few locations in western Massachusetts, but persist more widely in northern Vermont. Parasitism by the introduced braconid wasp Cotesia glomerata (L.) has been postulated as responsible for this decline. Field exposures of cohorts of P. napi larvae in 2002 showed that, on the summer host plant Sisymbrium officinale (L.) Scoop., parasitism rates of second generation butterfly larvae were very high (100% in Massachsusetts and 66% in Vermont). Direct observations of host plant and habitat use patterns by P. napi females in northern Vermont in 2000 showed that this species changes habitats between the first and second generation, with over 95% of eggs of the first generation of P. napi being laid in wooded habitats on the crucifer Cardamine (formerly Dentaria) diphylla (Michx.) Wood. Second generation butterflies fly in meadows and oviposit on S. officinale and other crucifers in full-sun habitats. The second flight of P. napi is, however, only a partial generation, with many first generation pupae entering diapause. The proportion of butterflies entering diapause increases if eggs are laid on C. diphylla plants at or past the flower bud stage. Of first instar P. napi reared outdoors on pre-flower-bud C. diphylla, 63% (n=64) entered diapause in Massachusetts, but 86% (n=119) did so in northern Vermont. Higher rates of diapause in early larval groups in northern Vermont, plus lower rates of parasitism of second generation larvae in meadows, as compared to Massachusetts, indicate that the impact of C. glomerata on total population survival is lower in Vermont and is likely the reason P. napi has persisted in northern Vermont, but not in western Massachusetts. This case illustrates how non-target effects of parasitoids may be mediated by habitat and life history features of populations of affected insects, which may differ geographically.
Pieris napi oleracea Harris is a native pierid butterfly that has suffered a range reduction in New England that began after the invasion of its range by the non-native congener Pieris rapae L. and one of its braconid parasitoids, Cotesia glomerata (L.). P. napi has nearly disappeared from Massachusetts, but remains common in northern Vermont. We investigated food plant abundance and Cotesia spp. larval parasitism as possible factors to explain the historical changes in P. napi’s distribution. We found that the current range of P. napi was not explained by the abundance of its key first generation food plant (two-leafed toothwort, Cardamine diphylla [Michx.]). We also found that levels of Cotesia spp. parasitism in meadows in the second generation were similar in Vermont and Massachusetts. Further, we found that both C. glomerata and the related introduced Pieris spp. parasitoid Cotesia rubecula (Marshall) forage for hosts predominantly in sunny meadows and not in woods, where the first generation of P. napi occurs. We found that under field conditions in meadow habitats, C. glomerata parasitizes P. napi at higher rates than P. rapae. We postulate that the persistence of P. napi in Vermont and its disappearance in Massachusetts is caused by high parasitism of the second generation by C. glomerata in meadow habitats, coupled with a north–south cline in the rate of commitment of first generation P. napi pupae to diapause, such that northern populations act functionally as univoltine species developing in a parasitoid free habitat (woods), while southern populations acted as a bivoltine species and went extinct due to low survival in the second generation in meadows due to C. glomerata parasitism.
